Vol. 16 No. 2 (2021)
Articles

Bone histology of Broad-snouted Caiman Caiman latirostris (Crocodylia: Alligatoridae) as tool for morphophysiological inferences in Crocodylia

Paulo Braga Mascarenhas-Junior
Laboratório Interdisciplinar de Anfíbios e Répteis, Universidade Federal Rural de Pernambuco (UFRPE), Recife, Pernambuco
Luís Bassetti
Laboratório de Ecologia Isotópica – CENA/USP, Piracicaba, São Paulo
Juliana Manso Sayão
Museu Nacional do Rio de Janeiro, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Rio de Janeiro

Published 2021-11-05

Keywords

  • Crocodylians,
  • growth rate,
  • ontogeny,
  • osteohistology

How to Cite

Mascarenhas-Junior, P., Bassetti, L. A., & Manso Sayão, J. (2021). Bone histology of Broad-snouted Caiman Caiman latirostris (Crocodylia: Alligatoridae) as tool for morphophysiological inferences in Crocodylia. Acta Herpetologica, 16(2), 109–121. https://doi.org/10.36253/a_h-10079

Abstract

Bone histology is an important tool for the interpretation of life patterns in animals of the past and extant fauna. The crocodylians have been studied as important inferential models for morphophysiological characteristics. We aimed to characterize the osteohistology of captive Caiman latirostris, identifying its microanatomy related to growth rates, ontogeny, and environmental conditions. We analyzed five pairs of humeri (proximal elements of the appendicular skeleton) and ribs (axial skeleton) of females’ caiman. Ribs showed, in general, woven-fibered tissues, with low vascularization and parallel-fibered bone and many resorption and erosion cavities. It presented lines of arrested growth (LAGs) in three individuals, without skeletochronological compatibility. Humeri showed a gradient of woven-fibered to parallel-fibered and lamellar-zonal bone as the individuals aging. We observed compacted coarse cancellous bone (CCCB) and a higher number of LAGs in older specimens. Ribs remodel faster than humerus, showing an intra-individual histovariability. The humeri indicated an evident growth pattern with different ontogeny stages and growth rates in different ages. Fast-growing tissues are uncommon in crocodylians, but basal metabolism and optimal growth conditions can lead to this. Bone histology of C. latirostris shows patterns that can be used as inferential models for extant and extinct groups, but we encourage further studies for a better understanding, under different environmental conditions, such as temperature and food availability.

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References

Andrade R.C., Bantim, R.A.M., Lima, F.J., Campos, L.S., Eleutério, L.H.S., Sayão, J.M. (2015). New data about the presence and absence of the external fundamental system in archosaurs. Cadernos de Cultura e Ciência, 14(1): 200-211.
Andrade, R.C.L.P.D., Sena, M.V.A., Araújo, E.V., Bantim, R.A.M., Riff, D., Sayão, J.M. (2018). Osteohistological study on both fossil and living Caimaninae (Crocodyliformes, Crocodylia) from South America and preliminary comments on growth physiology and ecology. Historical Biology, 32(3): 346-355.
Brochu, C.A. (2010). A new alligatorid from the lower Eocene Green River Formation of Wyoming and the origin of caimans. Journal of Vertebrate Paleontology, 30(4): 1109-1126.
Caldwell, J. (2017). World trade in crocodilian skins 2013-2015. Louisiana, USA: The Louisiana Alligator Advisory Council.
Castanet, J., Francillon-Vieillot, H., Meunier, F.J., Ricqlès, A. (1993). Bone and individual aging. In: Bone, London: CRC press, 245–283.
Chinsamy, A., Codorniú, L., Chiappe, L. (2009). Palaeobiological implications of the bone histology of Pterodaustro guinazui. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 292(9): 1462-1477.
Chinsamy, A., Hillenius, W.J. (2004). Physiology of nonavian dinosaurs. In: The dinosauria, Berkeley: University of California Press, 643-659.
Chinsamy, A., Raath, M.A. (1992). Preparation of fossil bone for histological examination. Paleontologia Africana, 29(1): 39-44.
Company, J., Pereda-Suberbiola, X. (2017). Long bone histology of a eusuchian crocodyliform from the Upper Cretaceous of Spain: Implications for growth strategy in extinct crocodiles. Cretaceous Research, 72:1-7.
Coutinho, M.E., Marioni, B., Farias, I.P., Verdade, L.M., Bassetti, L.A.B., Mendonça, S.H.S.T., Vieira, T.Q., Magnusson, W.E., Campos, Z. (2013). Avaliação do risco de extinção do jacaré-de-papo-amarelo Caiman latirostris (Daudin, 1802) no Brasil. Embrapa Pantanal-Artigo em periódico indexado (ALICE). 1: 13-20.
Cubo, J., Le Ro, N., Martinez-Maza, C., Montes, L. (2012). Paleohistological estimation of bone growth rate in extinct archosaurs. Paleobiology, 38(2): 335-349.
Andrade, R.C.L.P., Sayão, J.M. (2014). Paleohistology and lifestyle inferences of a dyrosaurid (Archosauria: Crocodylomorpha) from Paraíba Basin (Northeastern Brazil). PloS one, 9(7).
Diefenbach, C.O.D.C. (1988). Thermal and feeding relations of Caiman latirostris (Crocodylia: Reptilia). Comparative Biochemistry and Physiology Part A: Physiology, 89(2): 149-155.
Enlow, D.H., Brown, S.O. (1958). A comparative histological study of fossil and recent bone tissues. Part III. The Texas Journal of Science, 10(2): 187-230.
Enlow, D.H. (1969). The bone of reptiles. In: Biology of the Reptilia, London: Academic press, 1:45-80.
Fernandez, L.M., Arias, M., Khazan, E.S. (2015). Analysis of population density and distribution of spectacled caiman (Caiman crocodilus) in Caño Palma, northeast Costa Rica. Herpetological Conservation and Biology, 10(3): 959-968.
Filogonio, R., Assis, V.B., Coutinho, M.E. et al. 2010. Distribution of populations of broad-snouted caiman (Caiman latirostris, Daudin 1802, Alligatoridae) in the São Francisco River basin, Brazil. Brazilian Journal of Biology, 70(4): 961-968.
Fincatti, C.R., Verdade, L.M. (1999). Variação térmica microclimática em estufa plástica e sua aplicação para crescimento de filhotes de jacarés. In: Conservação e Manejo de Jacarés e Crocodilos da América Latina, Piracicaba: Fundação de Estudos Agrários Luiz de Queiroz, 1: 75-83.
Fittkau, E.J. (1973). Crocodiles and the nutrient metabolism of Amazonian waters. Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas, 4(1): 103-133.
Francillon-Vieillot, H., Buffrénil, V., Castanet, J., Meunier, G.F.J. (1990). Microstructure and mineralization of vertebrate skeletal tissues. In: Skeletal Biomineralization Patterns, Processes and Evolutionary Trends. New York: Van Nostrand Reinhold, 471–548.
Huttenlocker, A.K., Woodward, H.N., Hall, B.K. (2013). The biology of bone. In: Bone histology of fossil tetrapods. Berkley: University of California Press, 1: 13-34.
Hutton, J.M. (1986). Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia, 1986:2, 332-341.
INMET- Instituto Nacional de Meteorologia. (2018). Dados históricos: Banco de Dados Meteorológicos para Ensino e Pesquisa. Brasília. Available on: <http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep>. Access on October 03, 2018.
Klein, N., Scheyer, T., Tütken, T. (2009). Skeletochronology and isotopic analysis of a captive individual of Alligator mississippiensis Daudin, 1802. Fossil Record, 12(2): 121-131.
Lamm, E.T. (2013). Preparation and sectioning of specimens. In: Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation, Berkeley: University of California Press, 55-160.
Lang, J.W. (1987). Crocodilian thermal selection. In: Wildlife management: crocodiles and alligators, Surrey Beautty and Sons press, 317.
Lee, A.H. (2004). Histological organization and its relationship to function in the femur of Alligator mississippiensis. Journal of Anatomy, 204(3):197-207.
Mascarenhas Júnior, P.B., Santos, E.M., Correia, J.M.S. (2018). Diagnóstico dos resgates de jacarés na região metropoliana do Recife, Pernambuco. Revista Ibero-Americana de Ciências Ambientais, 9(4): 138-145.
Mascarenhas Júnior, P.B., Santos, E.M., Moura, G.J.B., Diniz, G.T.N., Correia, J.M.S. (2020). Space-time distribution of Caiman latirostris (Alligatoridae) in lentic area of Atlantic Forest, northeast of Brazil. Herpetology Notes, 13: 29-137.
Melo, M.T.Q. (2002). Dieta do Caiman latirostris no sul do Brasil. In: Verdade LM, Larriera, A. La conservación y manejo de los Crocodylia de America Latina. Santa Fé: Fundación Banco Bica, 2: 119-125.
Padian, K. (2011). Vertebrate palaeohistology then and now: A retrospective in the light of the contributions of Armand de Ricqlès. Comptes Rendus Palevol, 10(5-6): 303-309.
Reid, R.E.H. (1984). Primary bone and dinosaurian physiology. Geological Magazine, 121(6): 5 89-598.
Reid, R.E.H. (1990). Zonal “growth rings” in dinosaurs. Modern Geology, 15(1): 19-48.
Reid, R.E.H. (1997). How dinosaurs grew. In: The complete dinosaur, Bloomington: Indiana Academic Press 757 p.
Ricqlès, A., Padian, K., Horner, J.R. (2001). The bone histology of basal birds in phylogenetic and ontogenetic perspectives. In New perspectives on the origin and early evolution of birds: proceedings of the international symposium in honor of John H. Ostrom New Haven, CT: Peabody Museum of Natural History press, Yale University, 411-426.
Ricqlès, A.D., Horner, J.R., Padian, K. (1998). Growth dynamics of the hadrosaurid dinosaur Maiasaura peeblesorum. Journal of Vertebrate Paleontology, 18(Suppl 3): 72A.
Ricqlès, A.D. (1983). Cyclical growth in the long limb bones of a sauropod dinosaur. Acta Palaeontologica Polonica, 28(1-2).
Ricqlès, A.J., Padian, K., Horner, J.R. 2003. On the bone histology of some Triassic pseudosuchian archosaurs and related taxa. In Annales de Paléontologie, 89(2): 67-101.
Sarkis-Gonçalves, F., Miranda-Vilela, M.P., Bassetti, L.A.B., Verdade, L.M. (2001). Manejo de jacarés-de-papo-amarelo (Caiman latirostris) em cativeiro. In: A produção animal na visão dos brasileiros. Piracicaba: Sociedade Brasileira de Zootecnia, Piracicaba: Fealq, 565-579.
Sayão, J.M., Bantim, R.A.M, Andrade, R.C.L.P., Lima, F.J., Saraiva A.A.F., Figueiredo R.G., Kellner, A.W.A. 2016) Paleohistology of Susisuchus anatoceps (Crocodylomorpha, Neosuchia): comments on growth strategies and lifestyle. PloS one, 11(5): 16.
Schweitzer, M.H., Elsey, R.M., Dacke, C.G., Horner, J.R., Lamm, E.T. (2007). Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone?. Bone, 40(4): 1152-1158.
Sena, M.V.A., Andrade, R.C.L.P., Sayão, J.M., Oliveira, G.R. (2018). Bone microanatomy of Pepesuchus deiseae (Mesoeucrocodylia, Peirosauridae) reveals a mature individual from the Upper Cretaceous of Brazil. Cretaceous Research, 90: 335-348.
Silva, R.G. (2000). Introdução à bioclimatologia animal. São Paulo: Nobel press, 286 p.
Smith, E.N., Robertson, S., Davies, D.G. (1978). Cutaneous blood flow during heating and cooling in the American alligator. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 235(3): 160-167.
Staton, M.A. (1988). Studies on the use of fats and carbohydrates in the diet of American alligators (Alligator mississippiensis). Thesis (Ph.D)- Graduate Faculty of the University of Georgia, Georgia, 151p.
Storrs, G.W. (1993). Function and phylogeny in sauropterygian (Diapsida) evolution. American Journal of Science, 293(A):63.
Tucker, A.D. (1997). Validation of skeletochronology to determine age of freshwater crocodiles (Crocodylus johnstoni). Marine and Freshwater Research, 48(4): 343-351.
Tumarkin-Deratzian, A.R., Vann, D.R., Dodson, P. (2007). Growth and textural ageing in long bones of the American alligator Alligator mississippiensis (Crocodylia: Alligatoridae). Zoological Journal of the Linnean Society, 150(1): 1-39.
Verdade, L.M., Larriera, A., Piña, C.I. (2010). Broad-snouted caiman Caiman latirostris. Crocodiles Status Survey and Conservation Action Plan, 18: 22.
Verdade, L.M., Packer, I.U., Michelotti, F., Rangel, M.C. (1994). Thermoregulatory behavior of broad-snouted caiman (Caiman latirostris) under different thermal regimes. In: Workshop sobre conservación y manejo del yacare overo Caiman latirostris. Santa Fé, 84-89.
Verdade, L.M. (1995). Biologia reprodutiva do jacaré-de-papo-amarelo (Caiman latirostris) em São Paulo, Brasil. In: Conservación y manejo de los Crocodylia de America Latina, Santa Fé: Fundación Banco Bica, 1: 57-79.
Waskow, K., Mateus, O. (2017). Dorsal rib histology of dinosaurs and a crocodylomorph from western Portugal: skeletochronological implications on age determination and life history traits. Comptes. Rendus. Palevol., 16(4): 425-439.
Waskow, K., Sander, P.M. (2014). Growth record and histological variation in the dorsal ribs of Camarasaurus sp. (Sauropoda). Journal of Vertebrate Paleontology, 34(4): 852-869.
Wilson, L.E., Chin, K. (2014). Comparative osteohistology of Hesperornis with reference to pygoscelid penguins: the effects of climate and behaviour on avian bone microstructure. Royal Society open science, 1(3): 140245.
Woodward, H.N., Horner, J.R., Farlow, J.O. (2014). Quantification of intraskeletal histovariability in Alligator mississippiensis and implications for vertebrate osteohistology. PeerJ, 2:1-34
Zug, G.R., Vitt, L., Caldwell, J.P. (2001). Herpetology: an introductory biology of amphibians and reptiles. Academic press. 629 p.